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Neuroimmune connections in jejunal and ileal Peyer’s patches at various bovine ages: potential sites for prion neuroinvasion

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Abstract

During preclinical stages of cattle orally infected with bovine spongiform encephalopathy (BSE), the responsible agent is confined to ileal Peyer’s patches (IPP), namely in nerve fibers and in lymph follicles, before reaching the peripheral and central nervous systems. No infectivity has been reported in other bovine lymphoid organs, including jejunal Peyer’s patches (JPP). To determine the potential sites for prion neuroinvasion in IPP, we analyzed the mucosal innervation and the interface between nerve fibers and follicular dendritic cells (FDC), two dramatic influences on neuroinvasion. Bovine IPP were studied at three ages, viz., newborn calves, calves less than 12 months old, and bovines older than 24 months, and the parameters obtained were compared with those of JPP. No differences in innervation patterns between IPP and JPP were found. The major difference observed was that, in calves of less than 12 months, IPP were the major mucosal-associated lymphoid organ that possessed a large number of follicles with extended FDC networks. Using a panel of antibodies, we showed that PP in 24-month-old bovines were highly innervated at various strategic sites assumed to be involved in the invasion and replication of the BSE pathogen: the suprafollicular dome, T cell area, and germinal centers. In PP in calves of less than 12 months old, no nerve fibers positive for the neurofilament markers NF-L (70 kDa) and NF-H (200 kDa) were observed in contact with FDC. Thus, in view of the proportion of these protein subunits present in neurofilaments, the innervation of the germinal centers can be said to be an age-dependent dynamic process. This variation in innervation might influence the path of neuroinvasion and, thus, the susceptibility of bovines to the BSE agent.

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Acknowledgements

The SAF 32 antibody was kindly provided by Jacques Grassi. We thank Dr. P. Lausberg for allowing samples to be collected at the local abattoir.

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Authors and Affiliations

  1. Institute of Human Histology, Department of Morphology and Immunology, Faculty of Medicine, University of Liège, Liège, Belgium

    Valérie Defaweux, Gauthier Dorban, Nandini Falisse-Poirier, Sylvain Flandroy, Danièle Zorzi & Ernst Heinen

  2. Department of Morphology and Pathology, Laboratory of Animal Histology, Faculty of Veterinary Medicine, University of Liège, Liège, Belgium

    Nadine Antoine & Joëlle Piret

  3. Department of Morphology and Pathology, Laboratory of Anatomy, Faculty of Veterinary Medicine, University of Liège, Liège, Belgium

    Annick Gabriel & Olivier Jacqmot

  4. Prion Protein Research Center, Human Histology Laboratory, University of Liège, Tour de Pharmacie (Tour 4 du CHU), Étage +41, Avenue de l’Hôpital, B-4000, Liège 1 (Sart-Tilman), Belgium

    Valérie Defaweux

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  1. Valérie Defaweux
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  2. Gauthier Dorban
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  10. Ernst Heinen
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Correspondence to Valérie Defaweux.

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This work was supported by the Région Wallonne and by the Leon Frederiq Foundation.

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Defaweux, V., Dorban, G., Antoine, N. et al. Neuroimmune connections in jejunal and ileal Peyer’s patches at various bovine ages: potential sites for prion neuroinvasion. Cell Tissue Res 329, 35–44 (2007). https://doi.org/10.1007/s00441-007-0396-4

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  • DOI: https://doi.org/10.1007/s00441-007-0396-4

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